A rock-boring and rock-ingesting freshwater bivalve (shipworm) from the Philippines

Abstract

Shipworms are a group of wood-boring and wood-feeding bivalves of extraordinary economic, ecological and historical importance. Known in the literature since the fourth century BC, shipworms are both destructive pests and critical providers of ecosystem services. All previously described shipworms are obligate wood-borers, completing all or part of their life cycle in wood and most are thought to use wood as a primary source of nutrition. Here, we report and describe a new anatomically and morphologically divergent species of shipworm that bores in carbonate limestone rather than in woody substrates and lacks adaptations associated with wood-boring and wood digestion. The species is highly unusual in that it bores by ingesting rock and is among the very few known freshwater rock-boring macrobioeroders. The calcareous burrow linings of this species resemble fossil borings normally associated with bivalve bioerosion of wood substrates (ichnospecies Teredolites longissimus ) in marginal and fully marine settings. The occurrence of this newly recognized shipworm in a lithic substrate has implications for teredinid phylogeny and evolution, and interpreting palaeoenvironmental conditions based on fossil bioerosion features.

Secondary Metabolism in the Gill Microbiota of Shipworms (Teredinidae) as Revealed by Comparison of Metagenomes and Nearly Complete Symbiont Genomes

“…K. polythalamius lacks significant amounts of cellulolytic symbionts such as T. turnerae and instead contains Thiosocius teredinicola, which oxidizes sulfide and generates energy for the host (23). Other shipworms are found in solid rock and in seagrass (24,25). Thus, gill symbionts vary, but in all cases the symbionts appear to be essential to the survival of shipworms.…”

Symbiotic cooperation between freshwater rock-boring bivalves and microorganisms promotes silicate bioerosion

“…Second, rock boring can also occur mechanically through bioabrasion. Several lines of evidence support this mechanism, including (i) the microtexture of the shells, consisting of excavating ridges and rasping structures rendering bivalves comparable to a so-called "living lime" 12 , (ii) muscular adaptation, as described by Shipway et al 4 regarding the large posterior adductor muscle of the shipworm Lithoredo abatanica (Bivalvia: Teredinidae), (iii) experimental and modeling results of the stimulation of the muscles that control the rotation of the shells of the bivalves, which made it possible to accurately reproduce the shapes of burrows and scrape marks resulting from the boring by the bivalve Barnea candida (Bivalvia: Pholadidae) 10 . Finally, it is now generally admitted that both mechanical abrasion and chemical etching occur synergistically, especially for living organisms that bore in calcareous rocks, where the substrate is first weakened chemically, while individual grains are subsequently excavated mechanically from the boring 5,9 .…”

“…Bioerosion is a commonplace strategy developed by living organisms, which consists in boring hard substrates of various origins, including biological materials (e.g., wood, shells, and bones) 1 , mud 2 , rocks 3 and even synthetic materials. Depending on the nature of the substrate and the borer, bioerosion ensures a wide range of metabolic activities and ecosystem services, ranging from nutrition 4 to the creation of microhabitats protected from predators for themselves as well as for secondary dwellers 5 .…”

Shipworm bioerosion of lithic substrates in a freshwater setting, Abatan River, Philippines: Ichnologic, paleoenvironmental and biogeomorphical implications

“…New work completed as part of the Philippine Mollusk Symbiont International Collaboration Biodiversity Group (PMS-ICBG) expedition on the island of Bohol, Philippines, has led to the description and naming of a novel shipworm taxon that is responsible for extensive macrobioerosion of a lithic substrate (limestone) cropping out in the bed and banks beneath freshwaters of the Abatan River. This new taxon is described in detail elsewhere [12]. The objectives of this contribution are to: (1) describe the character of the substrates and the borings therein; (2) compare these shipworm borings with previously defined ichnotaxa commonly ascribed to bivalves; (3) discuss the implications of this new finding for paleoenvironmental inferences traditionally drawn from fossil occurrences of shipworms and/or their biogenic structures; and (4) address the potential roles of shipworms as ecosystem engineers and geomorphic agents in freshwater aquatic systems.…”

“…At the time of field observations (August 17–19, 2018), which were made just prior to the rainy season, maximum river depth was ~5 m, tidal range was ~50 cm, river widths varied from 5–10 m along the studied stretch, and waters were fresh; measured salinities remained <0.5 ppt through tidal cycles. Limestone outcrops on the river bed and low banks are heavily colonized (Fig 2C) by the shipworm Lithoredo abatanica [12] and variably coated with algae and strewn with loose bioeroded limestone cobbles and boulders (Fig 2B and 2D). Woody land plant roots (Fig 2E) and submerged logs (Fig 2F) are heavily colonized by the wood-boring shipworm Nausitora sp.…”